Ontogeny of the adrenal gland in the spiny mouse, with particular reference to production of the steroids cortisol and dehydroepiandrosterone

Endocrinology

Volumn 154, Issue 3, 2013, Pages 1190-1201

  Quinn, Tracey A ^a   Ratnayake, Udani ^a   Dickinson, Hayley ^a   Nguyen, Tri Hung ^b   McIntosh, Michelle ^b   Castillo Melendez, Margie ^a   Conley, Alan J ^c   Walker, David W ^a,b  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ALDOSTERONE; CORTICOSTERONE; CYTOCHROME B5; HYDROCORTISONE; NEUROFILAMENT PROTEIN; PRASTERONE; PREGNENOLONE; STEROID; STEROID 17ALPHA MONOOXYGENASE; SYNAPTOPHYSIN; TYROSINE 3 MONOOXYGENASE;

ADRENAL CORTEX; ADRENAL GLAND; ADRENAL MEDULLA; ALDOSTERONE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CELL DIFFERENTIATION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; EXPLANT; FEMALE; FETUS; FETUS CIRCULATION; GENE EXPRESSION; GESTATIONAL AGE; HYDROCORTISONE BLOOD LEVEL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MATERNAL PLASMA; MOUSE; NONHUMAN; ONTOGENY; PERINATAL PERIOD; PREGNANCY; PRENATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; ZONA FASCICULATA; ZONA GLOMERULOSA; ZONATION;

3-HYDROXYSTEROID DEHYDROGENASES; ADRENAL GLANDS; ANIMALS; ANIMALS, NEWBORN; CYTOCHROMES B5; DEHYDROEPIANDROSTERONE; FEMALE; FETAL BLOOD; GESTATIONAL AGE; HUMANS; HYDROCORTISONE; IMMUNOHISTOCHEMISTRY; MALE; MURINAE; PREGNANCY; STEROID 17-ALPHA-HYDROXYLASE;

EID: 84874644570     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1953     Document Type: Article

References (66)

1. Nguyen AD, Conley AJ. Adrenal androgens in humans and nonhuman primates: Production, zonation and regulation. Endocr Dev. 2008;13:33-54.
2. Sun HZ, Zang WJ, Zhou B, Xu L, Wu SF. DHEA suppresses longitudinal bone growth by acting directly at growth plate through estrogen receptors. Endocrinology. 2011;152(4):1423-1433.
3. Arnold JT, Blackman MR. Does DHEA exert direct effects on androgen and estrogen receptors, and does it promote or prevent prostate cancer? Endocrinology. 2005;146(11):4565-4567.
4. Mo Q, Lu S, Hu S, Simon NG. DHEA and DHEA sulfate differentially regulate neural androgen receptor and its transcriptional activity. Mol Brain Res. 2004;126(2):165-172.
5. Sacco M, Valenti G, Corvi Mora P, Wu FC, Ray DW. DHEA, a selective glucocorticoid receptor antagonist: Its role in immune system regulation and metabolism. J Endocrinol Invest. 2002;25 (10 Suppl):81-82.
6. May M, Holmes E, Rogers W, Poth M. Protection from glucocorticoid induced thymic involution by dehydroepiandrosterone. Life Sci. 1990;46(22):1627-1631.
7. Warren JC, Timberlake CE. Biosynthesis of estrogens in pregnancy: Precursor role of plasma dehydroisoandrosterone. Obstet Gynecol. 1964;23(5):689-698.
8. Giussani DA, Jenkins SL, Winter JA, Tame JD, Nathanielsz PW. Androstenedione treatment of pregnant baboons at 0.7-0.8 of gestation promotes a premature forward shift in the nocturnal maternal plasma estradiol surge relative to progesterone and increases myometrial contraction activity. Endocrinology. 2000;141(9):3296-3303.
9. Majewska MD. Neuronal actions of dehydroepiandrosterone possible roles in brain development, aging, memory, and affect. Ann N Y Acad Sci. 1995;774:111-120.
10. Cardounel A, RegelsonW,KalimiM.Dehydroepiandrosterone protects hippocampal neurons against neurotoxin-induced cell death: Mechanism of action. Proc Soc Exp Biol Med. 1999;222(2):145- 149.
11. Kimonides VG, Khatibi NH, Svendsen CN, Sofroniew MV, Herbert J. Dehydroepiandrosterone (DHEA) and DHEA-sulfate (DHEAS) protect hippocampal neurons against excitatory amino acid-induced neurotoxicity. Proc Natl Acad Sci U S A. 1998;95(4):1852-1857.
12. Kurata K, Takebayashi M, Morinobu S, Yamawaki S. α-Estradiol, dehydroepiandrosterone, and dehydroepiandrosterone sulfate protect against N-methyl-D-aspartate-induced neurotoxicity in rat hippocampal neurons by different mechanisms. J Pharmacol Exp Ther. 2004;311(1):237-245.
13. Kimonides VG, Spillantini MG, Sofroniew MV, Fawcett JW, Herbert J. Dehydroepiandrosterone antagonizes the neurotoxic effects of corticosterone and translocation of stress-activated protein kinase 3 in hippocampal primary cultures. Neuroscience. 1999;89(2): 429-436.
14. Brown RC, Han ZQ, Cascio C, Papadopoulos V. Oxidative stressmediated DHEA formation in Alzheimer's disease pathology. Neurobiol Aging. 2003;24(1):57-65.
15. KaminskaM,Harris J, Gijsbers K, Dubrovsky B. Dehydroepiandrosterone sulfate (DHEAS) counteracts decremental effects of corticosterone on dentate gyrus LTP. Implications for depression. Brain Res Bull. 2000;52(3):229-234.
16. Karishma KK, Herbert J. Dehydroepiandrosterone (DHEA) stimulates neurogenesis in the hippocampus of the rat, promotes survival of newly formed neurons and prevents corticosterone-induced suppression. Eur J Neurosci. 2002;16(3):445-453.
17. Marx CE, Stevens RD, Shampine LJ, et al. Neuroactive steroids are altered in schizophrenia and bipolar disorder: Relevance to pathophysiology and therapeutics. Neuropsychopharmacology. 2006; 31(6):1249-1263.
18. Ritsner M, Maayan R, Gibel A, Strous RD, Modai I, Weizman A. Elevation of the cortisol/dehydroepiandrosterone ratio in schizophrenia patients. Eur Neuropsychopharmacol. 2004;14:267-273.
19. Ritsner M, Maayan R, Gibel A, Weizman A. Differences in blood pregnenolone and dehydroepiandrosterone levels between schizophrenia patients and healthy subjects. Eur Neuropsychopharmacol. 2007;17:358-365.
20. Gallagher P, Watson S, Smith MS, Young AH, Ferrier IN. Plasma cortisol-dehydroepiandrosterone (DHEA) ratios in schizophrenia and bipolar disorder. Schizophr Res. 2007;90(1-3):258-265.
21. Pignatelli D, Xiao F, Gouveia AM, Ferreira JG, Vinson GP. Adrenarche in the rat. J Endocrinol. 2006;191(1):301-308.
22. Dickinson H, Walker DW, Wintour EM, Moritz K. Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse. Am J Physiol Regul Integr Comp Physiol. 2007;292(1):R453-R461.
23. LamersWH,Mooren PG, Griep H, Endert E, Degenhart HJ, Charles R. Hormones in perinatal rat and spiny mouse: Relation to altricial and precocial timing of birth.AmJ Physiol. 1986;251(1):E78-E85.
24. Parker CR, Staton B, Grilliot M. Ontogeny of cytochrome B-5 and cytochrome P450C17 in the human fetal adrenal gland during normal development. Endocr Res. 2004;30(4):541-542.
25. Kominami S, Ogawa N, Morimune R, Huang DY, Takemori S. The role of cytochrome-b5 in adrenal microsomal steroidogenesis. J Steroid Biochem Mol Biol. 1992;42(1):57-64.
26. Katagiri M, Kagawa N, Waterman MR. The role of cytochrome b5 in the biosynthesis of androgens by human P450c17. Arch Biochem Biophys. 1995;317(2):343-347.
27. Nguyen AD, Corbin CJ, Pattison JC, Bird IM, Conley AJ. The developmental increase in adrenocortical 17,20-lyase activity (biochemical adrenarche) is driven primarily by increasing cytochrome b5 in neonatal rhesus macaques. Endocrinology. 2009;150(4): 1748-1756.
28. Dickinson H, Walker D. Managing a colony of spiny mice (Acomys cahirinus) for perinatal research. ANZCART News. 2007;20(1): 4-11.
29. Bocking AD, McMillen IC, Harding R, Thorburn GD. Effect of reduced uterine blood-flow on fetal and maternal cortisol. J Dev Physiol. 1986;8(4):237-245.
30. De Peretti E, Forest MG. Unconjugated dehydroepiandrosterone plasma levels in normal subjects from birth to adolescence in human: The use of a sensitive radioimmunoassay. J Clin Endocrinol Metab. 1976;43(5):982-991.
31. Conley AJ, Bird IM. The role of cytochrome P450 17α-hydroxylase and 3α-hydroxysteroid dehydrogenase in the integration of gonadal and adrenal steroidogenesis via the-5 and-4 pathways of steroidogenesis in mammals. Biol Reprod. 1997;56(4):789-799.
32. Smith R, Mesiano S, Chan EC, Brown S, Jaffe RB. Corticotropinreleasing hormone directly and preferentially stimulates dehydroepiandrosterone sulfate secretion by human fetal adrenal cortical cells. J Clin Endocrinol Metab. 1998;83(8):2916-2920.
33. Kroboth PD, Salek FS, Pittenger AL, Fabian TJ, Frye RF.DHEAand DHEA-S: A review. J Clin Pharmacol. 1999;39(4):327-348.
34. Parker CR Jr. Dehydroepiandrosterone and dehydroepiandrosterone sulfate production in the human adrenal during development and aging. Steroids. 1999;64(9):640-647.
35. Parker LN. Adrenarche. The Endocrinologist. 1993;3(6):385-391.
36. Mapes S, Corbin CJ, Tarantal A, Conley A. The primate adrenal zona reticularis is definedbyexpression ofcytochromeb5,17α-hydroxylase/ 17,20-lyase cytochrome P450 (P450c17), and NADPH-cytochrome P450 reductase (reductase) but not 3α-hydroxysteroid dehydrogenase/ δ5-4 isomerase (3α-HSD). J Clin Endocrinol Metab. 1999;84(9): 3382-3385.
37. Neto AC, Ball BA, Browne P, Conley AJ. Cellular localization of androgen synthesis in equine granulosa-theca cell tumors: Immunohistochemical expression of 17α-hydroxylase/17,20-lyase cytochrome P450. Theriogenology. 2010;74(3):393-401.
38. Liu PS, Lin MK, Hsieh HL. Dehydroepiandrosterone sulfate inhibition of catecholamine secretion from bovine adrenal chromaffin cells. Neurosci Lett. 1996;204(3):181-184.
39. Charalampopoulos I, Dermitzaki E, Vardouli L, et al. Dehydroepiandrosterone sulfate and allopregnanolone directly stimulate catecholamine production via induction of tyrosine hydroxylase and secretion by affecting actin polymerization. Endocrinology. 2005; 146(8):3309-3318.
40. Chung KF, Qin N, Androutsellis-Theotokis A, Bornstein SR, Ehrhart-Bornstein M. Effects of dehydroepiandrosterone on proliferation and differentiation of chromaffin progenitor cells. Mol Cell Endocrinol. 2011;336(1-2):141-148.
41. Ducharme JR, ForestMG,Deperetti E, Sempe M, Collu R, Bertrand J. Plasma adrenal and gonadal sex steroids in human pubertal development. J Clin Endocrinol Metab. 1976;42(3):468-476.
42. Hyatt PJ, Bhatt K, Tait JF. Steroid-biosynthesis by zona fasciculata and zona reticularis cells purified from the mammalian adrenalcortex. J Steroid Biochem Mol Biol. 1983;19(1):953-959.
43. Rainey WE, Carr BR, Sasano H, Suzuki T, Mason JI. Dissecting human adrenal androgen production. Trends Endocrinol Metab. 2002;13(6):234-239.
44. Mesiano S, Jaffe RB. Developmental and functional biology of the primate fetal adrenal cortex. Endocr Rev. 1997;18(3):378-403.
45. Keegan CE, Hammer GD. Recent insights into organogenesis of the adrenal cortex. Trends Endocrinol Metab. 2002;13(5):200-208.
46. Beuschlein F, Keegan CE, Bavers DL, et al. SF-1, DAX-1, and ACD: Molecular determinants of adrenocortical growth and steroidogenesis. Endocr Res. 2002;28(4):597-607.
47. Dunn TB. Normal and pathologic anatomy of adrenal gland of mouse, including neoplasms. J Natl Cancer Inst. 1970;44(6):1323- 1389.
48. Shinzawa K, Ishibashi S, Murakoshi M, et al. Relationship between zonal distribution of microsomal cytochrome p-450s (p-45017-β, lyase and p-450c21) and steroidogenic activities in guinea-pig adrenal-cortex. J Endocrinol. 1988;119(2):191-200.
49. Legoascogne C, Sananes N, Gouezou M, et al. Immunoreactive cytochrome-p-450 17-β in rat and guinea-pig gonads, adrenal-glands and brain. J Reprod Fertil. 1991;93(2):609-622.
50. Boonstra R, Bradley AJ, Delehanty B. Preparing for hibernation in ground squirrels: Adrenal androgen production in summer linked to environmental severity in winter. Funct Ecol. 2011;25(6):1348-1359.
51. Boonstra R, Lane JE, Boutin S, Bradley A, Desantis L, Newman AEM, Soma KK. Plasma DHEA levels in wild, territorial red squirrels: Seasonal variation and effect of ACTH. Gen Comp Endocrinol. 2008;158(1):61-67.
52. Boonstra R, McColl CJ. Contrasting stress response of male arctic ground squirrels and red squirrels. J Exp Zool. 2000;286(4):390-404.
53. Pieper DR, Lobocki CA. Characterization of serum dehydroepiandrosterone secretion in golden hamsters. Proc Soc Exp Biol Med. 2000;224(4):278-284.
54. Belanger B, Couture J, Caron S, Bodou P, Fiet J, Belanger A. Production and secretion of C-19 steroids by rat and guinea pig adrenals. Steroids. 1990;55(8):360-365.
55. Ishimoto H, Jaffe RB. Development and function of the human fetal adrenal cortex: A key component in the feto-placental unit. Endocr Rev. 2011;32(3):317-355.
56. Miller WL. Steroid hormone biosynthesis and actions in the materno-feto-placental unit. Clin Perinatol. 1998;25:799-817.
57. Myers DA, Hyatt K, Mlynarczyk M, Bird IM, Ducsay CA. Longterm hypoxia represses the expression of key genes regulating cortisol biosynthesis in the near-term ovine fetus. Am J Physiol Regul Integr Comp Physiol. 2005;289(6):R1707-R1714.
58. Silver M, Fowden AL. Pituitary-adrenocortical activity in the fetal pig in the last third of gestation. Exp Physiol. 1989;74(2):197-206.
59. Liggins GC. Adrenocortical-related maturational events in fetus. Am J Obstet Gynecol. 1976;126(7):931-941.
60. Conrad CD, McLaughlin KJ, Harman JS, et al. Chronic glucocorticoids increase hippocampal vulnerability to neurotoxicity under conditions that produce CA3 dendritic retraction but fail to impair spatial recognition memory. J Neurosci. 2007;27(31):8278-8285.
61. Wolkowitz OM, Lupien SJ, Bigler ED. The -steroid dementia syndrome-: A possible model of human glucocorticoid neurotoxicity. Neurocase. 2007;13:189-200.
62. Herbert J. Neurosteroids, brain damage, and mental illness. Exp Gerontol. 1998;33(7-8):713-727.
63. Charalampopoulos I, Alexaki VI, Tsatsanis C, et al. Neurosteroids as endogenous inhibitors of neuronal cell apoptosis in aging. Neuroendocr Immune Crosstalk. 2006;1088:139-152.
64. Davis SR, Shah SM, McKenzie DP, Kulkarni J, Davison SL, Bell RJ. Dehydroepiandrosterone sulfate levels are associated with more favorable cognitive function in women. J Clin Endocrinol Metab. 2008;93(3):801-808.
65. Evans JG, Malouf R, Huppert F, van Niekerk JK. Dehydroepiandrosterone (DHEA) supplementation for cognitive function in healthy elderly people. Cochrane Database Syst Rev. 2006;CD006221(4).
66. Guazzo EP, Kirkpatrick PJ, Goodyer IM, Shiers HM, Herbert J. Cortisol, dehydroepiandrosterone (DHEA), and DHEA sulfate in the cerebrospinal fluid of man: Relation to blood levels and the effects of age. J Clin Endocrinol Metab. 1996;81(11):3951-3960.